Recently I wrote about the developmental hourglass pattern, which means that the most conserved developmental stages are not the earliest (as Karl von Baer thought at the dawn of comparative embryology), but some way into development. This pattern has been found in several animal phyla both at the morphological level and in various features of developmental gene expression, and it was recently also discovered in plants, which prompted my first post about it.

A group of researchers reckoned they should check how universal the hourglass is, and they thought the slime mould/social amoeba and honoured developmental model organism Dictyostelium is a good place to look (Tian et al., 2013). Unlike plants and animals, which develop from a single cell, the multicellular life stage of dictyostelids is a gathering of thousands of previously independent cells that may not be genetically identical. Therefore, these tiny creatures represent a very different approach to development from our favourite lab animals. Whether or not they still show an hourglass pattern could give clues about the deeper laws that govern all developmental processes.

Dictyostelids turn out to be complete deviants in this respect. Comparisons of the genes two species of Dictyostelium use in their multicellular development show neither von Baer’s “funnel” pattern of similarity nor an hourglass. If you include single-celled stages that aren’t, strictly speaking, “developmental”, similarities of gene expression give a “reverse hourglass” with lowest similarity in the middle. If you only consider the actual multicellular developmental stages, conservation increases towards the end – an “inverted funnel”. Other measures gave Tian et al. largely consistent results – genes expressed later in development were more likely to also be present in the other species, and their sequences were more similar on average.

Now that we have a pattern – what could explain it? The authors speculate that an idea that had been used to explain the hourglass in animals may apply just as well to the inverted funnel of slime moulds. This idea is that the evolvability of a developmental stage depends on the interactions that occur during it. The more interactions between genes/cells/tissues, the worse the effect of a tiny screw-up and the smaller the chance of a beneficial change, hence the most interconnected developmental stages will tend to be most conserved in evolution.

In animals, goes the reasoning, early development is relatively simple, and later development is relatively modular. Early on, there’s less to screw up, whereas later, every screw-up is limited to part of the embryo. In between is the sweet spot where everything talks to everything and a small modification can have large knock-on effects. The result is the hourglass. In slime moulds, however, that later stage when the developing organism is subdivided into semi-independent modules never comes. All tissues keep communicating and affecting each other right up to the point where the multicellular body is fully developed. Thus, if you like, only the first half of the hourglass happens in these creatures.

I recently wondered, in response to an “ideas” paper in BioEssays, whether animals, fungi, slime moulds etc. actually had a multicellular common ancestor. Dickinson and colleagues’ argument (partly) hinged on the shared presence of epithelia, “barrier” cell layers with distinct insides and outsides, in animals and the social amoeba Dictyostelium discoideum. The most recent crop from BioEssays includes a short letter by František Baluška of the botany department at the University of Bonn that challenges this argument.

Plants, Baluška reminds us, also have epithelia. These epithelia are functionally more similar to animals’ than the one Dickinson’s team found in the amoebae. While there may be doubts about amoebae, plants almost certainly became multicellular independently of animals. Ergo, convergent evolution can clearly produce similar tissues in two distant lineages. So why would we take the possession of an epithelium as evidence for a multicellular common ancestor?

Which is a perfectly valid argument, but it misses the point in my opinion.

The botanist writes,

[Plants] evolved their own plant-specific epithelia 3–5, obviously via convergent evolution. This fact alone not only continues to make plausible the traditional independent origin of multicellularity in the metazoa and social amoebae, but it also indicates that the power of convergent evolution should not be underestimated.

Of course it shouldn’t, but Dickinson’s team wasn’t arguing that “the traditional independent origin of multicelluarity” in animals and amoebae was not plausible any more. They find it unlikely that the functional and molecular similarity (does the latter exist between plants and animals?) between animal and amoeba epithelia is convergent, but they are suggesting that we investigate their new hypothesis, not that we summarily throw out the old one. Baluška is attacking a straw man.

Furthermore, he only addresses this one argument, but the thing in the Dickinson article that made me think the most was phylogeny. According to the traditional scenario, it seemed more likely that all those different unikont groups evolved multicellularity independently. But multicellularity is very widespread among unikonts, so precisely what makes the traditional scenario more likely? (Incidentally, has anyone done any actual statistics on this?)

As far as I’m concerned, the letter said nothing to change my mind. Dickinson et al. presented an interesting idea that’s definitely worth a closer look. I don’t think the evidence is currently strong enough to upset the consensus, but the proposal is not at all daft. I have to say I agree that plants should not be ignored, though. Because we can assume that any similarity between them and animals when it comes to being multicellular is the result of convergence, they’d be a wonderful “control group” when people start testing Dickinson et al.‘s hypothesis.

I think that’s something students of evolution should always keep in mind. Plants and animals have little reason to do things in the same way – they diverged very long ago, adapted to completely different lifestyles, etc. If they do so anyway, that might tell us something deeper about the way living things work. A limitation imposed by physics, a very ancient genetic predisposition, or simply the best way to do something – either way, finding the reason will enrich our knowledge of life and evolution. Animal scientists would be well advised to remember that.

Animals aren’t the only multicellular creatures in their phylogenetic neighbourhood. Social amoebae, many fungi and quite a few of the poorly known choanoflagellates spend at least part of their lives as collections of cooperating cells. Conventional wisdom has been that these groups invented multicellularity independently, but maybe conventional wisdom needs a bit of challenging.

To tell you the truth, I never really thought about the other possibility, that being multicellular is the original state of affair for these organisms. I never really considered the evidence on which the conventional wisdom was based. You could say I didn’t really care either way. A while back I saw a paper that said something about a social amoeba having an epithelium, but I just kind of shrugged and went on with my life. I don’t know, now an article in BioEssays brought this up again, and I’m not sure I was right to ignore it back then. I think Dickinson et al. (2012) have a point, and I think some assumptions may need to be reexamined.

In case you wondered, an epithelium is a type of tissue made of a layer or layers of polarised cells. “Polarised” means that various cellular components – proteins, attachments to neighbouring cells, organelles – are distributed unevenly in the cell, clustered towards one or the other side of the cell layer. Epithelia line pretty much everything in a typical animal’s body, from, well, the entire body, to things like guts and glands. They secrete important stuff like hormones, and their closely packed cells form a barrier to keep molecules and pathogens where they belong. An epithelium was thought to be a uniquely animal thing to have, but looking more closely at that weird little amoeba suggested it may not be.

The paper that I ignored was Dickinson et al. (2011) – yes, by the exact same people who wrote the BioEssays piece. OK, I didn’t completely ignore it. I read enough of it to scribble a quick note in my citation manager saying “screams convergent evolution to me”. The paper examined the multicellular stage in the life of Dictyostelium discoideum, an ordinarily single-celled amoeba that reacts to food shortages by crowding together with friends and family to form a fruiting body that helps disperse some of its cells in search of new habitats. The fruiting body is pretty complex for a “unicellular” creature, and it turns out that this complexity includes a region of tissue that looks quite a lot like a simple epithelium. It doesn’t just look like one; it sorts out its insides and outsides with the help of proteins called catenins, which are also involved in cell polarity in the epithelia of animals. (Below: D. discoideum being multicellular, from Wikipedia)

That isn’t much evidence to base an inference of homology on, especially since other key players in animal cell polarity are entirely absent from D. discoideum. But equally, the fact that tons of unikonts (the group including amoebae, slime moulds, fungi, choanoflagellates and animals) are single-celled doesn’t mean that the multicellular groups all came up with the idea independently. Evolution doesn’t always increase complexity – sometimes complexity becomes superfluous.

I remember when we discussed the choanoflagellate genome paper (King et al., 2008) in class. The genome in question belongs to a purportedly single-celled creature, but it contains tons of genes you’d think only multicellular organisms would need, such as genes for cell-to-cell adhesion proteins. So one explanation is that these proteins originally did something else, like anchoring a single cell to its favourite spot. Another explanation is that they did have something to do with multicellularity – it just wasn’t the multicellularity of animals at first.

This suggestion isn’t terribly controversial when you’re talking about choanoflagellates, since some of them do obviously form colonies (one such colony of Salpingoeca/Proterospongia rosetta is shown below, from Mark Dayel of the King lab via ChoanoWiki). It’s not hard to imagine that either the “single-celled” species whose genome was sequenced also has a colonial stage the scientists just never saw, or that its recent ancestors did.

Whether or not the same applies to the whole of unikonts is a more difficult question. I’m not at all familiar with the details of unikont relationships, but based on the tree shown in the BioEssays article, multicellularity is all over the group. In most cases, it’s facultative multicellularity; animals are rather the exception in being doomed to it for their entire lives. However, if you just looked at that tree, you’d wonder why the hell anyone thought the common ancestor of these things wasn’t some kind of multicellular.

Yet the details of animal-like multicellularity aren’t so widespread. True cadherins (the cell adhesion proteins I mentioned) have only been found in animals proper. Choanoflagellates and some even more obscure relatives of animals have bits and pieces of them, and other unikonts have none at all as far as anyone knows. Epithelium-like tissues have only been described in that one species of amoeba – but, as Dickinson and colleagues note, no one really looked in the others.

Personally, I wouldn’t be at all surprised if the conventional wisdom ended up shifting. I still don’t think that the evidence from Dictyostelium is enough to draw a conclusion. We obviously need to know a lot more about unikont genomes, tissues and life cycles to piece together the history of multicellularity in the group, but I’m not sure that right now a unicellular ancestor has a lot more going in its favour than a multicellular one. Guess we’ll have to wait and look with an open mind 🙂